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Phytochrome B Represses Teosinte Branched1 Expression and Induces Sorghum Axillary Bud Outgrowth in Response to Light Signals1

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Phytochrome B Represses Teosinte Branched1 Expression and Induces Sorghum Axillary Bud Outgrowth in Response to Light Signals1 Phytochrome B Represses Teosinte Branched1 Expression and Induces Sorghum Axillary Bud Outgrowth in Response to Light Signals1 Tesfamichael H. Kebrom, Byron L. Burson, and Scott A. Finlayson* Department of Soil and Crop Sciences (T.H.K., S.A.F.), and United States Department of Agriculture Agricultural Research Service (B.L.B.), Texas A&M University, College Station, Texas 77843–2474 Light is one of the environmental signals that regulate the development of shoot architecture. Molecular mechanisms regulating shoot branching by light signals have not been investigated in detail. Analyses of light signaling mutants defective in branching provide insight into the molecular events associated with the phenomenon. It is well documented that phytochrome B (phyB) mutant plants display constitutive shade avoidance responses, including increased plant height and enhanced apical dominance. We investigated the phyB-1 mutant sorghum (Sorghum bicolor) and analyzed the expression of the sorghum Teosinte Branched1 gene (SbTB1), which encodes a putative transcription factor that suppresses bud outgrowth, and the sorghum dormancy-associated gene (SbDRM1), a marker of bud dormancy. Buds are formed in the leaf axils of phyB-1; however, they enter into dormancy soon after their formation. The dormant state of phyB-1 buds is confirmed by the high level of expression of the SbDRM1 gene. The level of SbTB1 mRNA is higher in the buds of phyB-1 compared to wild type, suggesting that phyB mediates the growth of axillary shoots in response to light signals in part by regulating the mRNA abundance of SbTB1. These results are confirmed by growing wild-type seedlings with supplemental far-red light that induces shade avoidance responses. We hypothesize that active phyB (Pfr) suppresses the expression of the SbTB1 gene, thereby inducing bud outgrowth, whereas environmental conditions that inactivate phyB allow increased expression of SbTB1, thereby suppressing bud outgrowth. The highly ordered arrangement of leaves and in the axil of a leaf to form a bud (for review, see Ward branches and the final shoot architecture are associated and Leyser, 2004; McSteen and Leyser, 2005). Then, de- with a plant’s developmental strategy to ensure its pending on internal and environmental signals, the bud survival and productivity under continuously changing may continue growing to form an axillary shoot or enter growing conditions. A complex developmental pro- into dormancy. Different approaches have been used to gram that integrates genetic mechanisms, physiological study the regulation of axillary shoot development. processes, and environmental signals controls the over- Early decapitation studies and application of plant all form of the plant. The shoot architecture of crop hormones showed that auxin produced in the shoot plants has been modified during their domestication apex inhibits the outgrowth of axillary buds (Thimann and improvement. One of the great achievements in the and Skoog, 1933). Further research indicated that other history of crop improvement, ‘‘The Green Revolution,’’ plant hormones, such as cytokinins and abscisic acid, was due to dwarfing of wheat (Triticum aestivum)and are also involved in regulating branching (for review, other crops to increase nitrogen-use efficiency and re- see Stafstrom, 2000; Shimizu and Mori, 2001). duce lodging. A more complete understanding of the Molecular and genetic approaches have been used developmental programs that control shoot architec- to study the mechanisms of action of plant hormones ture will help to further improve resource-use effi- and to identify genes involved in regulating branch- ciency and yield of crop plants. ing. Genes that control axillary meristem initiation Shoot architecture is largely determined by the num- have been identified in various species (Schumacher ber of axillary shoots produced. Axillary shoot devel- et al., 1999; Greb et al., 2003; Li et al., 2003). Studies opment begins with the initiation of an axillary meristem using branching mutants of Arabidopsis (Arabidopsis thaliana), pea (Pisum sativum), and petunia (Petunia hybrida) are revealing the mechanisms of action of 1 This work was supported by the Texas Agricultural Experiment complex signaling networks of plant hormones that Station. regulate shoot branching (Leyser et al., 1993; Stirnberg * Corresponding author; e-mail sfi[email protected]; fax 979– et al., 1999; Booker et al., 2005; Foo et al., 2005; 845–0456. Snowden et al., 2005). Investigations using these mu- The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy tants suggest the presence of a novel, as yet uniden- described in the Instructions for Authors (www.plantphysiol.org) is: tified, plant hormone-like signal that integrates Scott A. Finlayson (sfi[email protected]). hormonal action during branching. Article, publication date, and citation information can be found at A genetic analysis of the morphological differences www.plantphysiol.org/cgi/doi/10.1104/pp.105.074856. between maize (Zea mays subsp. mays) and its wild Plant Physiology, March 2006, Vol. 140, pp. 1109–1117, www.plantphysiol.org Ó 2006 American Society of Plant Biologists 1109 Kebrom et al. developmental processes, including branching in sor- ghum (Sorghum bicolor) and Arabidopsis (Childs et al., 1992, 1997; Reed et al., 1993). We used the phyB null mutant sorghum (phyB-1)as a model for studying the regulation of branching by light. The strong apical dominance of phyB-1, and the early formation and ease of excising axillary buds make sorghum useful for studying the role of light in axillary shoot development. We asked whether light signals perceived by phyB control shoot branching by regulating the expression of branching genes previ- Figure 1. Median longitudinal sections of 4-d-old sorghum shoots. Arrows indicate buds in the axil of the first leaves of phyB-1 (A) and ously identified in other species. We characterized wild-type (B) sorghum seedlings. the enhanced apical dominance in phyB-1 sorghum and investigated the expression of branching-related genes, including the sorghum homologs of the TB1 ancestor teosinte (Zea mays subsp. parviglumis) led to (SbTB1) and dormancy-associated (SbDRM1) genes in the cloning of the Teosinte Branched1 (TB1)gene(Doebley phyB-1 and wild-type axillary buds. In this article, we et al., 1997). The TB1 gene encodes a putative basic report the regulation of expression of the sorghum helix-loop-helix transcription factor that is involved SbTB1 and SbDRM1 genes by light signals perceived in suppressing bud outgrowth (Doebley et al., 1997; by phyB, and phyB’s association with dormancy and Hubbard et al., 2002). An orthologous gene to maize outgrowth of axillary buds. TB1 was cloned from rice (Oryza sativa; OsTB1) and functions in a manner similar to the maize TB1 (Takeda et al., 2003). In both maize/teosinte and rice, RESULTS TB1 is expressed predominantly in the young axillary bud. Further studies of the functional properties of Enhanced Apical Dominance in phyB-1 Mutant Sorghum TB1 will provide insights regarding the regulation of shoot branching at the molecular level. The phyB-1 mutant sorghum fails to produce Several genes that are specifically up-regulated or branches during vegetative development, whereas down-regulated during branching have been identi- the near-isogenic wild-type plants branch profusely. fied. The dormancy-associated genes of pea, PsDRM1 The branching deficiency in phyB-1 could theoretically (Stafstrom et al., 1998b) and PsAD1 (Madoka and arise from either a defect in axillary meristem initia- Mori, 2000), are among the genes identified in cDNA tion or bud outgrowth. We found that the defect occurs libraries from dormant axillary buds. The mRNA abundance of PsDRM1 and PsAD1 in axillary buds declines after decapitation. However, while the ex- pression of these genes correlates strongly with bud dormancy, their functions are not known. It is well established that light quality (red:far red [R:FR]) is one of the environmental signals that regu- late shoot branching (Casal et al., 1986; Wan and Sosebee, 1998). However, little information exists re- garding the molecular mechanisms regulating shoot branching in response to light. Light signals may interact with plant hormones to regulate plant growth and development (Halliday and Fankhauser, 2003). Recent findings indicate that light and auxin interact in the regulation of adventitious root formation in Arabidopsis (Sorin et al., 2005). To fully understand the regulation of axillary shoot development, the in- teraction of light and hormonal and other environ- mental signals should be investigated. Plants use light signals perceived by photoreceptors to coordinate all stages of growth and development from germination to flowering. The phytochrome family of photoreceptors is involved in deetiolation, vegetative development, and flowering time in both dicots and monocots (Mathews and Sharrock, 1996; Figure 2. Bud length (A) and seedling height (B) of phyB-1 and wild- Sawers et al., 2005). Mutation in one of the family type sorghum. Inset shows bud length at 7 DAP, 8 DAP, and 9 DAP (not members, PHYTOCHROME B (PHYB), affects several visible in the main figure). Data are mean 6 SE; n 5 10. 1110 Plant Physiol. Vol. 140, 2006 PhyB Represses TB1 Expression and Induces Bud Outgrowth expressed in mature stems and roots. The Arabidopsis gene orthologous to PsDRM1, AtDRM1,hassimilar expression patterns to PsDRM1 (Stafstrom et al., 1998a; Tatematsu
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